Abstract

Filopodia are cellular protrusions that have been implicated in many types of mechanosensory activities. Morphogens are signaling proteins that regulate the patterned development of embryos and tissues. Both have long histories that date to the beginnings of cell and developmental biology in the early 20th century, but recent findings tie specialized filopodia called cytonemes to morphogen movement and morphogen signaling. This review explores the conceptual and experimental background for a model of paracrine signaling in which the exchange of morphogens between cells is directed to sites where cytonemes directly link cells that produce morphogens to cells that receive and respond to them. WIREs Dev Biol 2014, 3:445–463. doi: 10.1002/wdev.151 This article is categorized under: Establishment of Spatial and Temporal Patterns > Gradients Invertebrate Organogenesis > Flies

Images

Developmental induction revealed by grafting experiments in Hydra. When grafted onto the middle of the body of a healthy green hydra, transplantation of a white tentacle with peristome tissue at its base induces the host to produce ectopic tentacles. (Adapted from Ref .)

Hh and Dpp are transported by cytonemes in the wing disc. Depictions of transverse sections of the wing disc columnar epithelium showing that (a) basal cytonemes move Hh (blue) from the cells that make it in the posterior compartment to anterior compartment cells across the compartment border (dashed line) that activate Hh signal transduction and express Dpp (red). Dpp movement from the A/P signaling center is via apical cytonemes (b).

Topography of the third instar wing disc. This transverse optical section shows the highly folded shape of the wing disc that juxtaposes cells in space that are far apart within the columnar epithelial layer. (Adapted from Ref .)

A/P organizing centers of the wing disc columnar and peripodial epithelia. Frontal (top) and transverse (bottom) depictions of a wing disc and the distribution of Dpp from the organizing centers of each layer. The disc is a flattened sac and the Dpp organizing centers are not juxtaposed.

Homeotic transformation of the Drosophila antenna. The antenna to leg transformation in AntpR mutants (a) is incompletely penetrant such that individual flies have mosaics patches of transformed tissue (b). There is a precise correspondence between the location of the transformed patch and the type of leg structure in antenna‐leg chimeras. (Adapted from Ref .)

Induction in the Drosophila wing imaginal disc. The normal, wildtype wing disc (a) has an organizing center that expresses Dpp (red) in response to signaling by Hh (blue), which originates in the Posterior (P) compartment. Levels of Dpp and Hh across the disc are depicted in the graph below. A disc (b) with a clone in the P compartment that is deficient for engrailed function induces an ectopic organizing center and a duplication that includes both engrailed mutant and normal cells. Micrograph of wing with induced duplication and induced ectopic organizing center (c). (Adapted from Ref .)

Embryonic induction by Drosophila bicoid mRNA. bicoid mRNA is localized to the anterior pole in normal, wildtype Drosophila embryos, but injection of bicoid mRNA into the posterior pole induces the embryo to develop with head and thoracic structures closest to the site of injection. (Adapted from Ref .)

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